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Intraspecific variation and thermal acclimation effects on mitochondrial function in a eurythermal teleost (Fundulus heteroclitus) Chung-Chun-Lam, Dillon James

Abstract

Ambient temperature is a pervasive environmental stressor for ectotherms, with effects from individual atoms to the population level. Indeed, the effects of temperature on organismal performance are suggested to constrain species’ geographic distributions. Aerobic metabolism is proposed to underlie the thermal limits of organisms, with thermal constraints occurring at the level of the mitochondrion due to its position at the terminus of the O₂ transport cascade and as the primary site of cellular ATP production. Despite this theoretical link, there is limited understanding of the relationship between mitochondrial function and thermal tolerance, particularly for interacting responses among multiple biological timescales. I used two subspecies of Atlantic killifish (Fundulus heteroclitus) to characterize mitochondrial responses to acute thermal shifts following thermal acclimation to 5, 15, and 33 °C, and putative local adaptation. Northern killifish exhibited higher liver mitochondrial respiratory capacity and lower mitochondrial O2 binding affinity when compared to the southern subspecies. Subspecies variation in mitochondrial function was associated with differences in electron transport system (ETS) complex IV capacity. Decreasing acclimation temperature increased liver mitochondrial respiratory capacity and decreased mitochondrial O₂ binding affinity in both subspecies. Thermal acclimation effects on liver mitochondrial respiratory capacity were associated with ETS complex I. In contrast, heart and brain mitochondrial respiratory capacity decreased following acclimation to both high and low thermal extremes and did not differ between subspecies. Thermal acclimation effects on liver mitochondrial performance were not associated with increased reactive oxygen species production or a loss of mitochondrial proton motive force at high assay temperatures. Liver mitochondrial membrane composition varied in response to thermal acclimation and differed between subspecies, with thermal acclimation effects being largely consistent between subspecies. Mitochondrial lipid remodeling was primarily associated with changes in specific phospholipid species, suggesting a role for targeted membrane remodeling as a mechanism underlying variation in mitochondrial function. My data provide evidence for variation in mitochondrial function as a mechanism that differentiates aerobic and thermal performance between F. heteroclitus subspecies and that is involved in thermal acclimation responses. These mitochondrial responses likely underlie the aerobic performance limits of ectotherms and influence species’ fitness and geographic distributions.

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